Interaction of Cytochrome C and Its Precursor Apocytochrome C with Various Phospholipids

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1983 Jan 1

PMID 16453458

Citations 12

Authors

A Rietveld

P Sijens

A J Verkleij

B Kruijff

Affiliations

Soon will be listed here.

Abstract

The effects of cytochrome c and apocytochrome c on the structural properties of various membrane phospholipids in model systems were compared by binding, calorimetric, permeability, P n.m.r. and freeze-fracture experiments. Both cytochrome c and apocytochrome c experience strong interactions only with negatively charged phospholipids; apocytochrome c interacted more strongly than cytochrome c. These interactions are primarily electrostatic but also have a hydrophobic character. Cytochrome c as well as apocytochrome c induces changes in the structure of cardiolipin liposomes as is shown by P n.m.r. and freeze-fracture electron microscopy. Cytochrome c does not affect the bilayer structure of phosphatidylserine. In contrast, interaction of apocytochrome c with this phospholipid results in changes of the P n.m.r. bilayer spectrum of the liposomes and also particles are observed at the fracture faces. The results are discussed in relation to the import of the protein into the mitochondrion.

Citing Articles

Wheel and Deal in the Mitochondrial Inner Membranes: The Tale of Cytochrome and Cardiolipin.

Diaz-Quintana A, Perez-Mejias G, Guerra-Castellano A, De la Rosa M, Diaz-Moreno I Oxid Med Cell Longev. 2020; 2020:6813405.

PMID: 32377304 PMC: 7193304. DOI: 10.1155/2020/6813405.

Method for measuring the unbinding energy of strongly-bound membrane-associated proteins.

Bauve E, Vernon B, Ye D, Rogers D, Siegrist C, Carson B Biochim Biophys Acta. 2016; 1858(11):2753-2762.

PMID: 27425029 PMC: 5266593. DOI: 10.1016/j.bbamem.2016.07.004.

Structural transformations of cytochrome c upon interaction with cardiolipin.

Muenzner J, Pletneva E Chem Phys Lipids. 2013; 179:57-63.

PMID: 24252639 PMC: 3979421. DOI: 10.1016/j.chemphyslip.2013.11.002.

Thioredoxins, glutaredoxins, and peroxiredoxins--molecular mechanisms and health significance: from cofactors to antioxidants to redox signaling.

Hanschmann E, Godoy J, Berndt C, Hudemann C, Lillig C Antioxid Redox Signal. 2013; 19(13):1539-605.

PMID: 23397885 PMC: 3797455. DOI: 10.1089/ars.2012.4599.

The role of hydrophobic interactions in positioning of peripheral proteins in membranes.

Lomize A, Pogozheva I, Lomize M, Mosberg H BMC Struct Biol. 2007; 7:44.

PMID: 17603894 PMC: 1934363. DOI: 10.1186/1472-6807-7-44.

References

Papahadjopoulos D, Moscarello M, Eylar E, Isac T . Effects of proteins on thermotropic phase transitions of phospholipid membranes. Biochim Biophys Acta. 1975; 401(3):317-35. DOI: 10.1016/0005-2736(75)90233-3. View

de Kruijff B . 13C NMR studies on [4-13C] cholesterol incorporated in sonicated phosphatidylcholine vesicles. Biochim Biophys Acta. 1978; 506(2):173-82. DOI: 10.1016/0005-2736(78)90388-7. View

Mombers C, Verkleij A, de Gier J, Van Deenen L . The interaction of spectrin-actin and synthetic phospholipids. II. The interaction with phosphatidylserine. Biochim Biophys Acta. 1979; 551(2):271-81. DOI: 10.1016/0005-2736(89)90005-9. View

Comfurius P, ZWAAL R . The enzymatic synthesis of phosphatidylserine and purification by CM-cellulose column chromatography. Biochim Biophys Acta. 1977; 488(1):36-42. DOI: 10.1016/0005-2760(77)90120-5. View

Deamer D, Bangham A . Large volume liposomes by an ether vaporization method. Biochim Biophys Acta. 1976; 443(3):629-34. DOI: 10.1016/0005-2736(76)90483-1. View

Blok M, Van Deenen L, de Gier J . The effect of chain length and lipid phase transitions on the selective permeability properties of liposomes. Biochim Biophys Acta. 1975; 406(2):187-96. DOI: 10.1016/0005-2736(75)90003-6. View

STOFFEL W, SCHIEFER H . Biosynthesis and composition of phosphatides in outer and inner mitochondrial membranes. Hoppe Seylers Z Physiol Chem. 1968; 349(8):1017-26. DOI: 10.1515/bchm2.1968.349.2.1017. View

FISHER W, Taniuchi H, ANFINSEN C . On the role of heme in the formation of the structure of cytochrome c. J Biol Chem. 1973; 248(9):3188-95. View

Nicholls P . Cytochrome c binding to enzymes and membranes. Biochim Biophys Acta. 1974; 346(3-4):261-310. DOI: 10.1016/0304-4173(74)90003-2. View

10.

Zimmermann R, Hennig B, Neupert W . Different transport pathways of individual precursor proteins in mitochondria. Eur J Biochem. 1981; 116(3):455-60. DOI: 10.1111/j.1432-1033.1981.tb05357.x. View

11.

Matsuura S, Arpin M, Hannum C, MARGOLIASH E, Sabatini D, Morimoto T . In vitro synthesis and posttranslational uptake of cytochrome c into isolated mitochondria: role of a specific addressing signal in the apocytochrome. Proc Natl Acad Sci U S A. 1981; 78(7):4368-72. PMC: 319791. DOI: 10.1073/pnas.78.7.4368. View

12.

Hennig B, Neupert W . Assembly of cytochrome c. Apocytochrome c is bound to specific sites on mitochondria before its conversion to holocytochrome c. Eur J Biochem. 1981; 121(1):203-12. DOI: 10.1111/j.1432-1033.1981.tb06450.x. View

13.

Takano T, DICKERSON R . Conformation change of cytochrome c. II. Ferricytochrome c refinement at 1.8 A and comparison with the ferrocytochrome structure. J Mol Biol. 1981; 153(1):95-115. DOI: 10.1016/0022-2836(81)90529-5. View

14.

Pscheid P, Schudt C, Plattner H . Cryofixation of monolayer cell cultures for freeze-fracturing without chemical pre-treatments. J Microsc. 1981; 121(Pt 2):149-67. DOI: 10.1111/j.1365-2818.1981.tb01208.x. View

15.

Seelig J, Seelig A . Lipid conformation in model membranes and biological membranes. Q Rev Biophys. 1980; 13(1):19-61. DOI: 10.1017/s0033583500000305. View

16.

Hille J, Sauve P, DE HAAS G, Egmond M . Physicochemical studies on the interaction of pancreatic phospholipase A2 with a micellar substrate analogue. Biochemistry. 1981; 20(14):4068-73. DOI: 10.1021/bi00517a019. View

17.

Van Dijck P, VERVERGAERT P, Verkleij A, Van Deenen L, de Gier J . Influence of Ca2+ and Mg2+ on the thermotropic behaviour and permeability properties of liposomes prepared from dimyristoyl phosphatidylglycerol and mixtures of dimyristoyl phosphatidylglycerol and dimyristoyl phosphatidylcholine. Biochim Biophys Acta. 1975; 406(4):465-78. DOI: 10.1016/0005-2736(75)90025-5. View

18.

Stellwagen E, Rysavy R, Babul G . The conformation of horse heart apocytochrome c. J Biol Chem. 1972; 247(24):8074-7. View

19.

Cohen J, FISHER W, Schechter A . Spectroscopic studies on the conformation of cytochrome c and apocytochrome c. J Biol Chem. 1974; 249(4):1113-8. View

20.

Kimelberg H, Papahadjopoulos D . Phospholipid-protein interactions: membrane permeability correlated with monolayer "penetration". Biochim Biophys Acta. 1971; 233(3):805-9. DOI: 10.1016/0005-2736(71)90181-7. View